Cyclotides insert into lipid bilayers to form membrane pores and destabilize the membrane through hydrophobic and phosphoethanolamine-specific interactions

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43884-43898

  Wang, Conan K ^a   Wacklin, Hanna P ^b,c   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

^c EUROPEAN SPALLATION SOURCE ERIC   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BILAYER MEMBRANES; CIRCULAR PROTEINS; COMPLEX FORMATIONS; CRITICAL COMPONENT; CYCLOTIDES; FREE ENERGY OF BINDING; HYDROPHOBIC FORCES; ISOTHERMAL TITRATION CALORIMETRY; KALATA B1; MECHANISM OF ACTION; MEMBRANE PORES; MEMBRANE SURFACE; NEUTRON REFLECTOMETRY; OUTER MEMBRANE; PORE FORMATION; SEQUENCE DIVERSITY; SPECIFIC BINDING; THERAPEUTIC APPLICATION;

HYDROPHOBICITY; LIPID BILAYERS;

MEMBRANES;

CYCLOTIDE; DODECYLPHOSPHORYLCHOLINE; PHOSPHOETHANOLAMINE;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; ENTROPY; HYDROPHOBICITY; ISOTHERMAL TITRATION CALORIMETRY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE BIOLOGY; MEMBRANE DESTABILIZATION; MEMBRANE LEAFLET; MICELLE; MOLECULAR DYNAMICS; NUCLEAR PORE; PRIORITY JOURNAL; QUARTZ CRYSTAL MICROBALANCE; REFLECTOMETRY; SURFACE PROPERTY; THERMODYNAMICS;

CYCLOTIDES; ETHANOLAMINES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; OLDENLANDIA; PLANT PROTEINS; PROTEIN BINDING;

EID: 84871548747     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421198     Document Type: Article

References (59)

1. Craik, D. J., Daly, N. L., Bond, T., and Waine, C. (1999) Plant cyclotides. A unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J. Mol. Biol. 294, 1327-1336 (Pubitemid 30008803)
2. Gruber, C. W., Elliott, A. G., Ireland, D. C., Delprete, P. G., Dessein, S., Göransson, U., Trabi, M., Wang, C. K., Kinghorn, A. B., Robbrecht, E., and Craik, D. J. (2008) Distribution and evolution of circular miniproteins in flowering plants. Plant Cell 20, 2471-2483 (Pubitemid 352844612)
3. Simonsen, S. M., Sando, L., Ireland, D. C., Colgrave, M. L., Bharathi, R., Göransson, U., and Craik, D. J. (2005) A continent of plant defense peptide diversity. Cyclotides in Australian Hybanthus (Violaceae). Plant Cell 17, 3176-3189
4. Wang, C. K., Kaas, Q., Chiche, L., and Craik, D. J. (2008) CyBase. A database of cyclic protein sequences and structures, with applications in protein discovery and engineering. Nucleic Acids Res. 36, D206-210 (Pubitemid 351149723)
5. Poth, A. G., Colgrave, M. L., Lyons, R. E., Daly, N. L., and Craik, D. J. (2011) Discovery of an unusual biosynthetic origin for circular proteins in legumes. Proc. Natl. Acad. Sci. U.S.A. 108, 10127-10132
6. Göransson, U., Burman, R., Gunasekera, S., Strömstedt, A. A., and Rosengren, K. J. (2012) Circular proteins from plants and fungi. J. Biol. Chem. 287, 27001-27006
7. Nguyen, G. K., Lim, W. H., Nguyen, P. Q., and Tam, J. P. (2012) Novel cyclotides and uncyclotides with highly shortened precursors from Chassalia chartacea and effects of methionine oxidation on bioactivities. J. Biol. Chem. 287, 17598-17607
8. Pinto, M. F., Fensterseifer, I. C., Migliolo, L., Sousa, D. A., de Capdville, G., Arboleda-Valencia, J. W., Colgrave, M. L., Craik, D. J., Magalhães, B. S., Dias, S. C., and Franco, O. L. (2012) Identification and structural characterization of novel cyclotide with activity against an insect pest of sugar cane. J. Biol. Chem. 287, 134-147
9. Tang, J., Wang, C. K., Pan, X., Yan, H., Zeng, G., Xu, W., He, W., Daly, N. L., Craik, D. J., and Tan, N. (2010) Isolation and characterization of cytotoxic cyclotides from Viola tricolor. Peptides 31, 1434-1440
10. Mulvenna, J. P., Mylne, J. S., Bharathi, R., Burton, R. A., Shirley, N. J., Fincher, G. B., Anderson, M. A., and Craik, D. J. (2006) Discovery of cyclotide-like protein sequences in graminaceous crop plants. Ancestral precursors of circular proteins? Plant Cell 18, 2134-2144 (Pubitemid 44484715)
11. Colgrave, M. L., and Craik, D. J. (2004) Thermal, chemical, and enzymatic stability of the cyclotide kalata B1. The importance of the cyclic cystine knot. Biochemistry 43, 5965-5975 (Pubitemid 38669464)
12. Craik, D. J., Cěmažar, M., and Daly, N. L. (2006) The cyclotides and related macrocyclic peptides as scaffolds in drug design. Curr. Opin. Drug Discov. Dev. 9, 251-260 (Pubitemid 35012711)
13. Saether, O., Craik, D. J., Campbell, I. D., Sletten, K., Juul, J., and Norman, D. G. (1995) Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry 34, 4147-4158
14. Gran, L. (1973) Oxytocic principles of Oldenlandia affinis. Lloydia 36, 174-178
15. Gustafson, K. R., McKee, T. C., and Bokesch, H. R. (2004) Anti-HIV cyclotides. Curr. Protein Pept. Sci. 5, 331-340 (Pubitemid 39200163)
16. Tam, J. P., Lu, Y. A., Yang, J. L., and Chiu, K. W. (1999) An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides. Proc. Natl. Acad. Sci. U.S.A. 96, 8913-8918 (Pubitemid 29374682)
17. Schöpke, T., Hasan Agha, M. I., Kraft, R., Otto, A., and Hiller, K. (1993) Hamolytisch aktive Komponenten aus Viola tricolor L. und Viola arvensis Murray. Sci. Pharm. 61, 145-153 (Pubitemid 23244214)
18. Göransson, U., Svangård, E., Claeson, P., and Bohlin, L. (2004) Novel strategies for isolation and characterization of cyclotides. The discovery of bioactive macrocyclic plant polypeptides in the Violaceae. Curr. Protein Pept. Sci. 5, 317-329 (Pubitemid 39200162)
19. Witherup, K. M., Bogusky, M. J., Anderson, P. S., Ramjit, H., Ransom, R. W., Wood, T., and Sardana, M. (1994) Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes. J. Nat. Prod. 57, 1619-1625
20. Plan, M. R., Saska, I., Cagauan, A. G., and Craik, D. J. (2008) Backbone cyclised peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J. Agric. Food Chem. 56, 5237-5241 (Pubitemid 352039129)
21. Colgrave, M. L., Kotze, A. C., Huang, Y. H., O'Grady, J., Simonsen, S. M., and Craik, D. J. (2008) Cyclotides. Natural, circular plant peptides that possess significant activity against gastrointestinal nematode parasites of sheep. Biochemistry 47, 5581-5589 (Pubitemid 351705169)
22. Colgrave, M. L., Kotze, A. C., Ireland, D. C., Wang, C. K., and Craik, D. J. (2008) The anthelmintic activity of the cyclotides. Natural variants with enhanced activity. Chembiochem 9, 1939-1945
23. Jennings, C., West, J., Waine, C., Craik, D., and Anderson, M. (2001) Biosynthesis and insecticidal properties of plant cyclotides. The cyclic knotted proteins from Oldenlandia affinis. Proc. Natl. Acad. Sci. U.S.A. 98, 10614-10619 (Pubitemid 32878669)
24. Jennings, C. V., Rosengren, K. J., Daly, N. L., Plan, M., Stevens, J., Scanlon, M. J., Waine, C., Norman, D. G., Anderson, M. A., and Craik, D. J. (2005) Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist. Do Möbius strips exist in nature? Biochemistry 44, 851-860 (Pubitemid 40129645)
25. Barbeta, B. L., Marshall, A. T., Gillon, A. D., Craik, D. J., and Anderson, M. A. (2008) Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proc. Natl. Acad. Sci. U.S.A. 105, 1221-1225 (Pubitemid 351397034)
26. Kamimori, H., Hall, K., Craik, D. J., and Aguilar, M. I. (2005) Studies on the membrane interactions of the cyclotides kalata B1 and kalata B6 on model membrane systems by surface plasmon resonance. Anal. Biochem. 337, 149-153 (Pubitemid 40092791)
27. Henriques, S. T., Huang, Y. H., Rosengren, K. J., Franquelim, H. G., Carvalho, F. A., Johnson, A., Sonza, S., Tachedjian, G., Castanho, M. A., Daly, N. L., and Craik, D. J. (2011) Decoding the membrane activity of the cyclotide kalata B1. The importance of phosphatidylethanolamine phospholipids and lipid organization on hemolytic and anti-HIV activities. J. Biol. Chem. 286, 24231-24241
28. Henriques, S. T., Huang, Y. H., Castanho, M. A., Bagatolli, L. A., Sonza, S., Tachedjian, G., Daly, N. L., and Craik, D. J. (2012) Phosphatidylethanolamine binding is a conserved feature of cyclotide-membrane interactions. J. Biol. Chem. 287, 33629-33643
29. Huang, Y. H., Colgrave, M. L., Daly, N. L., Keleshian, A., Martinac, B., and Craik, D. J. (2009) The biological activity of the prototypic cyclotide kalata b1 is modulated by the formation of multimeric pores. J. Biol. Chem. 284, 20699-20707
30. Sando, L., Henriques, S. T., Foley, F., Simonsen, S. M., Daly, N. L., Hall, K. N., Gustafson, K. R., Aguilar, M. I., and Craik, D. J. (2011) A synthetic mirror image of kalata B1 reveals that cyclotide activity is independent of a protein receptor. Chembiochem 12, 2456-2462
31. 2+/DPC micelle. J. Inorg. Biochem. 102, 1246-1256
32. Shenkarev, Z. O., Nadezhdin, K. D., Sobol, V. A., Sobol, A. G., Skjeldal, L., and Arseniev, A. S. (2006) Conformation and mode of membrane interaction in cyclotides. Spatial structure of kalata B1 bound to a dodecylphosphocholine micelle. FEBS J. 273, 2658-2672
33. Nourse, A., Trabi, M., Daly, N. L., and Craik, D. J. (2004) A comparison of the self-association behavior of the plant cyclotides kalata B1 and kalata B2 via analytical ultracentrifugation. J. Biol. Chem. 279, 562-570 (Pubitemid 38044859)
34. Mulvenna, J. P., Wang, C., and Craik, D. J. (2006) CyBase. A database of cyclic protein sequence and structure. Nucleic Acids Res. 34, D192-D194
35. Daly, N. L., Love, S., Alewood, P. F., and Craik, D. J. (1999) Chemical synthesis and folding pathways of large cyclic polypeptides. Studies of the cystine knot polypeptide kalata B1. Biochemistry 38, 10606-10614
36. Tam, J. P., Lu, Y.-A., and Yu, Q. (1999) Thia zip reaction for synthesis of large cyclic peptides: mechanisms and applications. J. Am. Chem. Soc. 121, 4316-4324
37. Silvius, J. R. (1986) Solid- and liquid-phase equilibria in phosphatidylcholine/phosphatidylethanolamine mixtures. A calorimetric study. Biochim. Biophys. Acta 857, 217-228
38. Penfold, J. (1991) Instrumentation for neutron reflectivity. Physica B 173, 1-10
39. Vacklin, H. P., Tiberg, F., Fragneto, G., and Thomas, R. K. (2005) Composition of supported model membranes determined by neutron reflection. Langmuir 21, 2827-2837 (Pubitemid 40448945)
40. Vacklin, H. P., Tiberg, F., Fragneto, G., and Thomas, R. K. (2005) Phospholipase A2 hydrolysis of supported phospholipid bilayers. A neutron reflectivity and ellipsometry study. Biochemistry 44, 2811-2821 (Pubitemid 40293657)
41. Nelson, A. (2006) Co-refinement of multiple-contrast neutron/X-ray reflectivity data using MOTOFIT. J. Appl. Crystallogr. 39, 273-276
42. Heavens, O. S. (1955) Optical properties of Thin Films, Dover Publications, London
43. Armen, R. S., Uitto, O. D., and Feller, S. E. (1998) Phospholipid component volumes: determination and application to bilayer structure calculations. Biophys. J. 75, 734-744 (Pubitemid 28357515)
44. Zamyatin, A. A. (1972) Protein volume in solution. Prog. Biophys. Mol. Biol. 24, 107-123
45. Skjeldal, L., Gran, L., Sletten, K., and Volkman, B. F. (2002) Refined structure and metal binding site of the kalata B1 peptide. Arch. Biochem. Biophys. 399, 142-148 (Pubitemid 34848600)
46. Simonsen, S. M., Sando, L., Rosengren, K. J., Wang, C. K., Colgrave, M. L., Daly, N. L., and Craik, D. J. (2008) Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity. J. Biol. Chem. 283, 9805-9813
47. Simonsen, S. M., Daly, N. L., and Craik, D. J. (2004) Capped acyclic permutants of the circular protein kalata B1. FEBS Lett. 577, 399-402 (Pubitemid 39535321)
48. Craik, D. J., Simonsen, S., and Daly, N. L. (2002) The cyclotides. Novel macrocyclic peptides as scaffolds in drug design. Curr. Opin. Drug Discov. Devel. 5, 251-260 (Pubitemid 35012711)
49. Gould, A., Ji, Y., Aboye, T. L., and Camarero, J. A. (2011) Cyclotides, a novel ultrastable polypeptide scaffold for drug discovery. Curr. Pharm. Des. 17, 4294-4307
50. Thongyoo, P., Bonomelli, C., Leatherbarrow, R. J., and Tate, E. W. (2009) Potent inhibitors of β-tryptase and human leukocyte elastase based on the MCoTI-II scaffold. J. Med. Chem. 52, 6197-6200
51. Chan, L. Y., Gunasekera, S., Henriques, S. T., Worth, N. F., Le, S. J., Clark, R. J., Campbell, J. H., Craik, D. J., and Daly, N. L. (2011) Engineering pro-angiogenic peptides using stable, disulfide-rich cyclic scaffolds. Blood 118, 6709-6717
52. Wong, C. T., Rowlands, D. K., Wong, C. H., Lo, T. W., Nguyen, G. K., Li, H. Y., and Tam, J. P. (2012) Orally active peptidic bradykinin B1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment. Angew. Chem. Int. Ed. Engl. 51, 5620-5624
53. Seelig, J. (2004) Thermodynamics of lipid-peptide interactions. Biochim. Biophys. Acta 1666, 40-50
54. Fernández-Vidal, M., White, S. H., and Ladokhin, A. S. (2011) Membrane partitioning: "classical" and "nonclassical" hydrophobic effects. J. Membr. Biol. 239, 5-14
55. Wang, C. K., Colgrave, M. L., Gustafson, K. R., Ireland, D. C., Goransson, U., and Craik, D. J. (2008) Anti-HIV cyclotides from the Chinese medicinal herb Viola yedoensis. J. Nat. Prod. 71, 47-52 (Pubitemid 351236394)
56. Parisi, M., Li, R., and Oliver, B. (2011) Lipid profiles of female and male Drosophila. BMC Res. Notes 4, 198
57. Greenwood, K. P., Daly, N. L., Brown, D. L., Stow, J. L., and Craik, D. J. (2007) The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Int. J. Biochem. Cell Biol. 39, 2252-2264 (Pubitemid 47484280)
58. Brogden, K. A. (2005) Antimicrobial peptides. Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250
59. Ludtke, S. J., He, K., Heller, W. T., Harroun, T. A., Yang, L., and Huang, H. W. (1996) Membrane pores induced by magainin. Biochemistry 35, 13723-13728 (Pubitemid 26363914)